Long-term Trends in Tuberculosis Comparison of Age-cohort Data between Hong Kong and England and Wales KAREN TOCQUE, MARK A. BELLIS, CHEUK M. TAM, SHIU L. CHAN, QUTUB SYED, TRACEY REMMINGTON, and PETER D. O. DAVIES Communicable Disease Surveillance Center (North West), Public Health Laboratory, Fazakerley Hospital; Department of Public Health, John Moores University; Tuberculosis Research Unit, Cardiothoracic Centre, Liverpool, United Kingdom; Department of Health Chest Service, Wanchai Polyclinic, Hong Kong, Republic of China
The caseload of tuberculosis in developing countries is increasingly associated with the elderly. This is possibly due to increased longevity today and a change in the lifetime risk of tuberculosis within birth cohorts. Published data for tuberculosis notifications for Hong Kong and England and Wales have been used to calculate age-specific rates of disease by different age groups for different birth cohorts. In Hong Kong, each birth cohort showed a similar pattern of disease by age, with rates peaking in the 25 to 39-yr age groups and gradually declining thereafter. After 1978, regardless of age at that time, all age cohorts showed an increase in tuberculosis rates with increasing age. This trend was more marked in males than females. A similar pattern was seen for birth cohorts in England and Wales except that the peak occurred earlier in life (before 25 yr of age) and the decline with age ceased in 1984. Thereafter, rates increased in males born before 1930 but showed only a leveling off in females. If these data represent a true increase in tuberculosis rates, rather than resulting from a change in reporting accuracy and completeness, the burden of tuberculosis in the elderly is likely to continue to increase substantially. Tocque K, Bellis MA, Tam CM, Chan SL, Syed Q, Remmington T, Davies PDO. Long-term trends in tuberculosis: comparison of age-cohort data between Hong Kong and England and Wales. AM J RESPIR CRIT CARE MED 1998;158:484–488.
Cases of tuberculosis in the developed countries of the world have declined steadily since records were first collected, until the mid-1980s. A characteristic epidemiologic feature associated with a decreasing incidence of the disease has been a concomitant increase in the proportion of older patients (1–4). This was particularly dramatic after the introduction of chemotherapy in the 1950s, when transmission of the Mycobacterium to the young was significantly reduced (5). A clearer picture of tuberculosis risks over time is gained from birth-cohort analysis. The first published works to use this approach were those of Andvord (1930) (6) for Denmark, England, and Norway and those of Frost (1939) (7) for Massachusetts, USA. In 1950, Springett (8) compared a similar analysis for England and Wales, Scotland, Ireland, and Paris, France. These three studies recorded mortality curves of very similar shapes for each successive birth cohort, with a peak mortality in those 20 to 30 yr of age, a steady decline with age thereafter, and progressively lower mortality for each birth cohort at any given age. More recent work in Finland and Sweden (9) has shown a similar pattern. These studies have shown that the apparent increasing risk of tuberculosis in the elderly did not result from a postponement of risk to later life but from a residual of a higher risk from earlier life (7).
The resurgence in tuberculosis in recent years in many developed countries, including England and Wales (10–13) and the United States (14, 15), may have altered this pattern of disease incidence by age. The aim of the present study was to compare the age-related pattern of tuberculosis in different birth cohorts in Hong Kong with rates in similar birth cohorts in England and Wales, where tuberculosis notifications are approximately 10 times lower, to determine whether risk of disease may now be changing with increased longevity.
METHODS The case definition of tuberculosis in both Hong Kong and England and Wales is the same, namely, that a clinician who “believes the patient to be suffering from tuberculosis” has a statutory obligation to report the patient to the local government authority.
Hong Kong Data Tuberculosis notification rates by age and sex between 1958 and 1993 were obtained from the Annual Reports of the Chest Service of the Department of Health (Hong Kong Government) (14). The annual data were broken down into 5-yr age categories, and notification rates at 5-yr intervals only were analyzed (1958, 1963, 1968, 1973, 1978, 1983, 1988, and 1993).
England and Wales Data (Received in original form September 30, 1997 and in revised form March 16, 1998) Supported by The Smith Charity. Correspondence and requests for reprints should be addressed to Karen Tocque, Fazakerley Hospital, CDSC (North West), Public Health Laboratory, Lower Lane, Liverpool L97AL, UK. E-mail:
[email protected] Am J Respir Crit Care Med Vol 158. pp 484–488, 1998 Internet address: www.atsjournals.org
Published notifications of tuberculosis by age and sex and midyear population estimates from 1954 to 1994 were obtained from the relevant annual monitors published by the Office of Population Censuses and Surveys (OPCS) (15) and used to calculate rates of tuberculosis for each age group. Because tuberculosis notification data in England and Wales are categorized into 10-yr age groups, data at 10-yr intervals only were used to calculate tuberculosis rates for specific birth co-
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Tocque, Bellis, Tam, et al.: Long-term Trends in Tuberculosis horts over time. Before 1964, data for those 25 yr of age and older were categorized into 20-yr age groups. Therefore, to maintain the consistency of birth cohorts, data for 5 to 14 and 15 to 24 age groups only were available prior to 1964. These years represent the earliest for which published data are available.
RESULTS Notifications over Time
Tuberculosis notifications, for all forms of disease, in both Hong Kong and England and Wales showed an overall decline with time (Figure 1). In Hong Kong, the general decline was more gradual than in England and Wales and was interrupted in 1967 when tuberculosis statistics were reorganized. A smaller interruption in the decline occurred in 1979 when there was an influx of Vietnamese refugees (14). In England and Wales, the decline was steady and rapid between 1954 and 1968 (approximately 9% per year) and more gradual thereafter (3% per year). The incidence of tuberculosis in Hong Kong males was characteristically 8 to 15 times higher than those in England and Wales and 6 to 10 times higher in females. Age-dependent tuberculosis rates also showed a decrease over time, but with the smallest relative decreases occurring in the oldest age groups—those older than 65 yr of age. Tuberculosis rates for specific birth cohorts were determined from these age distributions, as illustrated in Figure 2. Thus, as each
Figure 2. Age-incidence curves for male tuberculosis cases in Hong Kong from 1958 to 1993. Arrows illustrate how rates were calculated for two individual birth cohorts as examples of how the data were derived for Figures 3 and 4.
time period moved on 5 yr (for Hong Kong) or 10 yr (for England and Wales), the rate of disease for each cohort moved into the next 5-yr or 10-yr age category, respectively. Patterns of Disease in Birth Cohorts
Hong Kong. From the annual age distributions of tuberculosis, the patterns of disease for 13 different birth cohorts (born
Figure 1. Tuberculosis notifications (all forms) in the male (closed circles) and female (asterisks) populations of England and Wales from 1954 to 1994 (top panel) and Hong Kong from 1957 to 1993 (bottom panel).
Figure 3. Age-specific pattern of tuberculosis in 13 cohorts born between 1909 to 1913 and 1969 to 1973 in Hong Kong. Males (top panel) and females (bottom panel).
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age in 1978. This was very clear in males (Figure 3, top panel) when the increase in rate began after the age of 35 to 39 in the cohort born 1939 to 1943, but not until after the age of 65 to 69 in the cohort born 1909 to 1913. In females, the rates did not increase but leveled off, and the year that this change took place was less clear than in males (Figure 3, bottom panel). England and Wales. The pattern of disease in eight birth cohorts (born 1890 to 1899 through to 1960 to 1969) were determined, spanning as much as 40 yr of life for each cohort (Figure 4). These showed a similar situation to that observed for Hong Kong, with a decline in tuberculosis rate at any given age for each successive cohort. However, where recorded, the peak incidence was earlier (younger than 25 yr of age) but with a gradual decline thereafter. The halt in this decline occurred after 1984 in England and Wales. By 1994, rates had either increased slightly (in males born before 1930) or leveled off (in males born between 1930 and 1950, and in females born before 1940). Quantification of Rate Changes
The change in rate between each successive age was calculated for cohorts born before 1949. The overall change in direction and magnitude of the rate change before and after the year when rates began to rise, as observed in Figures 3 and 4 (1978 in Hong Kong and 1982 in England and Wales), is shown in Table 1. In Hong Kong, there was a significant difference in rate change before and after 1978; median rates declining before 1978 and rising afterwards in both males and females. In England and Wales, there was a significant difference before and after 1982 only in males, and the median rate was still declining, but to a lesser extent than before 1982. Figure 4. Age-specific pattern of tuberculosis in eight cohorts born between 1890 to 1899 and 1960 to 1969 in males (top panel) and females (bottom panel) in England and Wales.
1909 to 1913 through to 1969 to 1973) were determined, spanning as much as 35 yr of life for each cohort (Figure 3). The pattern of tuberculosis incidence was very similar in both male and female cohorts, with a decline in rate at any given age for each successive birth cohort. Despite the successively lower rates, each age distribution showed a similar shape, with a peak incidence in those 25 to 39 yr of age and a gradual decline with age thereafter, until 1978 when the decline with age halted (e.g., those in birth cohort born 1939 to 1943 were 35 to 39 yr of age in 1978, and those in birth cohort born 1944 to 1948 were 30 to 34 yr of age). After 1978, an increase in tuberculosis rate with age occurred in all cohorts, irrespective of the
DISCUSSION This study has shown that after a previous decline in the risk of tuberculosis with age in all birth cohorts, after 1978 in Hong Kong, the risk increased with age in all cohorts born before 1944 and stopped declining in those born between 1944 and 1953. Similarly, in England and Wales, the risk of tuberculosis stopped declining with age after 1984 in all cohorts born before 1950. In all previous birth-cohort studies (6–9), the rate of tuberculosis declined continuously with age after peak rates in those 20 to 30 yr of age, irrespective of year of birth. Thus, this study is the first time that an increasing risk of tuberculosis with increasing age of specific birth cohorts has been observed. If this phenomenon is not due to factitious causes such as overreporting of cases, it reveals that the epidemiologic features of tuberculosis are indeed altering. This change in risk
TABLE 1 RATE CHANGES BETWEEN SUCCESSIVE AGE CATEGORIES FOR ALL COHORTS BORN BEFORE 1949* Median Rate Change with Successive Age Categories Before 1978 (n 5 27)
After 1978 (n 5 16)
Hong Kong
Males† Females†
2166.4 (IQR: 2212.6 to 283.9) 267.6 (IQR: 2112.5 to 226.0)
31.2 (IQR: 13 to 51.7) 2.7 (IQR: 210.3 to 19.8)
England and Wales
Males‡ Females§
226.1 (IQR: 231.9 to 219.9) 213.1 (IQR: 222.0 to 24.7)
Before 1982 (n 5 4)
* Values are medians, with interquartile ranges (IQR) shown in parentheses. † p , 0.001, Kruskal-Wallis sign rank test. ‡ p , 0.005, Kruskal-Wallis sign rank test. § p , 0.064, Kruskal-Wallis sign rank test.
After 1982 (n 5 9) 27.2 (IQR: 214.1 to 0.8) 24.5 (IQR: 27.8 to 20.4)
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with increasing age would mean that, in Hong Kong in particular, tuberculosis rates in all age groups are likely to continue to increase with aging. Thus, as life expectancy improves, an even larger tuberculosis burden in the elderly is likely to increase transmission of infection and disease to all age groups. It is possible that these data may not represent a true rise in cases because of several factors. First, immigration from high prevalence countries may play a part in higher levels of disease in recent years. However, in England and Wales, a greater number of cases in immigrants are observed in younger age groups; therefore, immigration would be unlikely to contribute to higher rates in older ages. Also, although there was an influx of Vietnamese refugees into Hong Kong in 1979, present day immigrants come from more affluent sections of the Chinese population and are unlikely to contribute significantly to tuberculosis rates. If immigration were a major factor, the change in cohort pattern would have taken place gradually over several years, rather than over the short time period found in this study. Second, underreporting or overreporting in previous years could alter the apparent trend in tuberculosis rates today. Reporting completeness in London and elsewhere in the United Kingdom may only have been around 73% in the 1980s (16–18), but has apparently improved greatly since (19). Changes in reporting completeness will lead to an apparent alteration in the epidemiology of the disease. Chemoprophylaxis cases have been omitted from records since 1982. However, this cannot explain the observed change in risk occurring around 10 yr later because the rates changed in older age groups, which do not normally received chemoprophylaxis. Third, overreporting now could result in an apparently higher rate in all age groups. It is possible that increased awareness after the halt in the decline of overall tuberculosis rates in 1987 and onward has taken a few years to filter through. Nonetheless, changes in reporting completeness are unlikely since there has been no change in case definition until 1996 (20). In the UK, higher apparent rates may have resulted from increased awareness of tuberculosis leading to an increased diagnosis of the disease in all ages or indeed over reporting tuberculosis cases which are never de-notified (21). However, the change in the risk of disease with age occurred in Hong Kong between 1978 and 1983, when the global interest in tuberculosis had not yet begun. Although it is not known whether the influx of refugees from Vietnam in 1979 affected not only the rates of disease in all age cohorts but also local interest and awareness of the tuberculosis. Nevertheless, it is unlikely that this influx could explain the continual rise in risk of tuberculosis in all birth cohorts that was still observed until 1993. Thus, the increasing rates in older age groups of all cohorts probably represent real epidemiologic changes because of changes in the biology of tuberculosis infection. Older patients may be becoming reinfected with disease at a time when their immune system is partially compromised because of aging (18). The fact that the Hong Kong rates showed an appreciable rise compared with those of England and Wales may be due to a greater risk of reinfection because of the higher incidence of tuberculosis in the Hong Kong community. Davies (4) has pointed out that, among the white population in England and Wales, tuberculosis rates in older females declined more slowly than in males, perhaps as a result of increased infection during the war years. The role played by the elimination of M. bovis and by routine milk pasteurization since 1950 may have played an important part in the rapid decline of incidence in cohorts born after this time. Reactivation of M. tuberculosis, and also maybe M. bovis, in those exposed before 1950 may now be occurring as immunity declines with age: a
trend that has not been apparent until recently, when longevity increased. A real change in disease patterns has serious implications for an increased burden of tuberculosis in the elderly. This phenomenon is likely to be present, and increasing, in other rapidly emerging economies of the Pacific rim as life expectation improves. The elderly have an increased chance of cavitating disease and therefore of sputum positivity, rendering them a pool of infection within the community (22). The greater increase in disease rates in developing countries may impinge on developed countries because of migration (23), but it is also likely that the same continued increase will occur in the England and Wales population. Furthermore, HIVrelated tuberculosis (which is currently low in England and Wales at around 3%) tends to occur in younger age groups, and this has drawn attention away from tuberculosis in the older age groups. It is this risk, with consequences for transmission in the community, that we still cannot afford to ignore. References 1. Grigg, E. R. M. 1958. The arcana of tuberculosis. Am. Rev. Tuberc. 78: 151–172. 2. Powell, K. E., and L. S. Farer. 1980. The rising age of the tuberculosis patient: a sign of success or failure. J. Infect. Dis. 142:946–948. 3. Stead, W. W., and J. P. Lofgren. 1983. Does the risk of tuberculosis increase with old age? J. Infect. Dis. 147:951–955. 4. Davies, P. D. O. 1989. The slowing of the decline in tuberculosis notifications and HIV infections. Respir. Med. 83:321–322. 5. Regan, M., K. Tocque, M. A. Bellis, Q. Syed, and P. D. O. Davies. 1995. Tuberculin positivity in Liverpool schoolchildren 1954 to 1990: a measure of transmission following the introduction of chemotherapy (abstract). Thorax 50(Suppl.):A60. 6. Andvord, K. F. 1930. What can be learned following the development of tuberculosis from generation to generation (translated by Dr. Gerard Wijsmuller). Norsk Mag. Laegevidensk. 91:642–660. 7. Frost, H. 1995. The age selection of mortality from tuberculosis in successive decades: 1939 historical paper. Am. J. Epidemiol. 141:91–96. 8. Springett, V. H. 1950. A comparative study of tuberculosis mortality rates. J. Hyg. 48:361–395. 9. Haro, A. S. 1994. Cohort approach in tuberculosis surveillance: comparison of the situation in Sweden and Finland. Tuber. Lung Dis. 75:271–282. 10. Doherty, M. J., D. P. S. Spence, and P. D. O. Davies. 1995. The increase in tuberculosis notifications in England and Wales since 1987. Tuber. Lung Dis. 76:196–200. 11. Onorato, I. M., J. H. Kent, and K. G. Castro. 1995. Epidemiology of tuberculosis. In L. I. Lutwick, editor. Tuberculosis: A Clinical Handbook. Chapman & Hall, New York. 21–53. 12. Hayward, A. C., and J. M. Watson. 1995. Tuberculosis in England and Wales 1982–1993: notifications exceeded predictions. CDR Rev. 5: R29–R33. 13. Sudre, P., G. Ten Dam, and A. Kochi. 1992. Tuberculosis: a global overview of the situation today. Bull. WHO 70:149–159. 14. Chest Service of the Government Department of Health. 1993. Annual Report, Hong Kong. 15. Communicable Diseases Monitors. Series MB2. Year 1974–1994. Office of Population Censuses and Surveys. HMSO, London. 1976–1996. 16. Sheldon, C. D., K. King, H. Cock, P. Wilkinson, and N. C. Barnes. 1992. Notifications of tuberculosis: how many cases are never reported? Thorax 47:1015–1018. 17. Bradley, B. L., K. M. Kerr, A. D. Lutch, and D. Lamb. 1988. Notification of tuberculosis: can the pathologist help? B.M.J. 297:595. 18. Woo, J., H. S. Chan, C. B. Haslett, P. C. Ho, R. Chan, A. Sham, and P. D. O. Davies. 1996. Tuberculosis among elderly Chinese in residential homes: tuberculin reactivity and estimated prevalence. Gerontology 42:155–162. 19. Brown, J. S., F. Wells, G. Duckworth, E. A. Paul, and N. C. Barnes. 1995. Improving notification rates or tuberculosis. B.M.J. 310:974. 20. Schaberg, T. 1996. Epidemiology of tuberculosis in Europe: still a matter of deep concern. Eur. J. Respir. Med. 9:866–869. 21. Mangtani, P., L. Rodirgues, and J. Watson. 1985. Laboratory reports of opportunistic and other mycobacterial infections and their relation-
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gland & Wales, 1978–9. B.M.J. 281:895–898. 23. Nisar, M., C. S. D. Williams, and P. D. O. Davies. 1991. Experience of tuberculosis in immigrants from South East Asia: implications for the imminent lease back of Hong Kong. Respir. Med. 85:319–322.
